PTH1 Receptor Is Involved in Mediating Cellular Response to Long-Chain Polyunsaturated Fatty Acids

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Candelario, Jose ^a   Tavakoli, Hesam ^a   Chachisvilis, Mirianas ^a  

^a LA JOLLA BIOENGINEERING INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOCOSAHEXAENOIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; ICOSAPENTAENOIC ACID; LONG CHAIN FATTY ACID; LONG CHAIN POLYUNSATURATED FATTY ACID; MITOGEN ACTIVATED PROTEIN KINASE; PARATHYROID HORMONE RECEPTOR 1; PARATHYROID HORMONE[1-34]; POLYUNSATURATED FATTY ACID; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ANIMAL CELL; ANISOTROPY; ARTICLE; BINDING COMPETITION; CELL ACTIVATION; CELL DIFFERENTIATION; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FATTY ACID ANALYSIS; FATTY ACID DESATURATION; FATTY ACID SYNTHESIS; FLUORESCENCE MICROSCOPY; GENE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NONHUMAN; PARATHYROID HORMONE RECEPTOR 1 GENE; PROTEIN CONFORMATION; PROTEIN EXPRESSION;

3T3 CELLS; AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CELL SURVIVAL; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOCOSAHEXAENOIC ACIDS; DRUG SYNERGISM; EICOSAPENTAENOIC ACID; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MOLECULAR SEQUENCE DATA; OSTEOBLASTS; PARATHYROID HORMONE; PARATHYROID HORMONE-RELATED PROTEIN; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, PARATHYROID HORMONE, TYPE 1; RNA, SMALL INTERFERING;

EID: 84871642853     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052583     Document Type: Article

References (72)

1. Ensrud KE, Palermo L, Black DM, Cauley J, Jergas M, et al. (1995) Hip and calcaneal bone loss increase with advancing age: Longitudinal results from the study of osteoporotic fractures. J Bone Miner Res 10: 1778-1787.
2. Rossignol M, Moride Y, Perreault S, Boivin JF, Ste-Marie LG, et al. (2002) Recommendations for the prevention of osteoporosis and fragility fractures. International comparison and synthesis. Int J Technol Assess Health Care 18: 597-610.
3. Abellan van Kan G, Gambassi G, de Groot LC, Andrieu S, Cederholm T, et al. (2008) Nutrition and aging. The Carla Workshop. The journal of nutrition, health & aging 12: 355-364.
4. Poole KE, Reeve J, (2005) Parathyroid hormone- a bone anabolic and catabolic agent. Curr Opin Pharmacol 5: 612-617.
5. Juppner H, Gardella T, Kronenberg H, Potts J Jr (2001) Endocrinology (DeGroot L, and Jameson J, eds). 2: 969-1053.
6. Strewler GJ, (2000) The physiology of parathyroid hormone-related protein. N Engl J Med 342: 177-185.
7. Mahon MJ, Bonacci TM, Divieti P, Smrcka AV, (2006) A docking site for G protein betagamma subunits on the parathyroid hormone 1 receptor supports signaling through multiple pathways. Mol endocrinol 20: 136-146.
8. Bastepe M, Weinstein LS, Ogata N, Kawaguchi H, Juppner H, et al. (2004) Stimulatory G protein directly regulates hypertrophic differentiation of growth plate cartilage in vivo. Proc Natl Acad Sci U S A 101: 14794-14799.
9. Mahon MJ, Donowitz M, Yun CC, Segre GV, (2002) Na(+)/H(+) exchanger regulatory factor 2 directs parathyroid hormone 1 receptor signalling. Nature 417: 858-861.
10. Datta NS, Abou-Samra AB, (2009) PTH and PTHrP signaling in osteoblasts. Cell Signal 21: 1245-1254.
11. Weinstein RS, Jilka RL, Almeida M, Roberson PK, Manolagas SC, (2010) Intermittent parathyroid hormone administration counteracts the adverse effects of glucocorticoids on osteoblast and osteocyte viability, bone formation, and strength in mice. Endocrinology 151: 2641-2649.
12. Mukherjee A, Rotwein P, (2009) Akt promotes BMP2-mediated osteoblast differentiation and bone development. J Cell Sci 122: 716-726.
13. Datta SR, Brunet A, Greenberg ME, (1999) Cellular survival: a play in three Akts. Genes Dev 13: 2905-2927.
14. Watkins BA, Lippman HE, Le Bouteiller L, Li Y, Seifert MF, (2001) Bioactive fatty acids: role in bone biology and bone cell function. Prog Lipid Res 40: 125-148.
15. Fernandes G, Bhattacharya A, Rahman M, Zaman K, Banu J, (2008) Effects of n-3 fatty acids on autoimmunity and osteoporosis. Front Biosci 13: 4015-4020.
16. Lavie CJ, Milani RV, Mehra MR, Ventura HO, (2009) Omega-3 polyunsaturated fatty acids and cardiovascular diseases. J Am Coll Cardiol 54: 585-594.
17. Poulsen RC, Moughan PJ, Kruger MC, (2007) Long-chain polyunsaturated fatty acids and the regulation of bone metabolism. Exp Biol Med (Maywood) 232: 1275-1288.
18. Coetzee M, Haag M, Joubert AM, Kruger MC, (2007) Effects of arachidonic acid, docosahexaenoic acid and prostaglandin E(2) on cell proliferation and morphology of MG-63 and MC3T3-E1 osteoblast-like cells. Prostaglandins Leukot Essent Fatty Acids 76: 35-45.
19. Bonnet N, Ferrari SL, (2011) Effects of long-term supplementation with omega-3 fatty acids on longitudinal changes in bone mass and microstructure in mice. J Nutr Biochem 22: 665-672.
20. Sakaguchi K, Morita I, Murota S, (1994) Eicosapentaenoic acid inhibits bone loss due to ovariectomy in rats. Prostaglandins Leukot Essent Fatty Acids 50: 81-84.
21. Kruger MC, Coetzer H, de Winter R, Gericke G, van Papendorp DH, (1998) Calcium, gamma-linolenic acid and eicosapentaenoic acid supplementation in senile osteoporosis. Aging 10: 385-394.
22. Shichikawa K, Takenaka Y, Maeda A, Yoshino R, Tsujimoto M, et al. (1981) A longitudinal population survey of rheumatoid arthritis in a rural district in Wakayama. Ryumachi [Rheumatism] 21 Suppl: 35-43.
23. Zwart SR, Pierson D, Mehta S, Gonda S, Smith SM, (2010) Capacity of Omega-3 Fatty Acids or Eicosapentaenoic Acid to Counteract Weightlessness-Induced Bone Loss by Inhibiting NF-kappa B Activation: From Cells to Bed Rest to Astronauts. J Bone Miner Res 25: 1049-1057.
24. Hogstrom M, Nordstrom P, Nordstrom A, (2007) n-3 fatty acids are positively associated with peak bone mineral density and bone accrual in healthy men: the NO2 Study. Am J Clin Nutr 85: 803-807.
25. Weiss LA, Barrett-Connor E, von Muhlen D, (2005) Ratio of n-6 to n-3 fatty acids and bone mineral density in older adults: the Rancho Bernardo study. Am J Clin Nutr 81: 934-938.
26. Kruger MC, Coetzer H, de Winter R, Claassen N, (1995) Eicosapentaenoic acid and docosahexaenoic acid supplementation increases calcium balance. Nutr Res 15: 211-219.
27. Schlemmer CK, Coetzer H, Claassen N, Kruger MC, (1999) Oestrogen and essential fatty acid supplementation corrects bone loss due to ovariectomy in the female Sprague Dawley rat. Prostaglandins Leukot Essent Fatty Acids 61: 381-390.
28. Li Y, Seifert MF, Lim SY, Salem N, Watkins BA, (2010) Bone mineral content is positively correlated to n-3 fatty acids in the femur of growing rats. Brit J Nutr 104: 674-685.
29. Hamilton JA, Kamp F, (1999) How are free fatty acids transported in membranes? Is it by proteins or by free diffusion through the lipids? Diabetes 48: 2255-2269.
30. Salem N Jr, Kim HY, and Yergey JA (1986) Docosahexaenoic Acid: Membrane Function and Metabolism. In: Simopoulos AP, Kifer RR, and Martin RE, editors. Health Effects of Polyunsaturated Fatty Acids in Seafoods. Academic Press: Academic Press. pp. 263-317.
31. VanMeter AR, Ehringer WD, Stillwell W, Blumenthal EJ, Jenski LJ, (1994) Aged lymphocyte proliferation following incorporation and retention of dietary omega-3 fatty acids. Mech Ageing Dev 75: 95-114.
32. Robinson DR, Xu LL, Knoell CT, Tateno S, Olesiak W, (1993) Modification of spleen phospholipid fatty acid composition by dietary fish oil and by n-3 fatty acid ethyl esters. J Lipid Res 34: 1423-1434.
33. Albert CM, Campos H, Stampfer MJ, Ridker PM, Manson JE, et al. (2002) Blood levels of long-chain n-3 fatty acids and the risk of sudden death. N Engl J Med 346: 1113-1118.
34. Leone TC, Weinheimer CJ, Kelly DP, (1999) A critical role for the peroxisome proliferator-activated receptor alpha (PPARalpha) in the cellular fasting response: the PPARalpha-null mouse as a model of fatty acid oxidation disorders. Proc Natl Acad Sci U S A 96: 7473-7478.
35. Fan YY, McMurray DN, Ly LH, Chapkin RS, (2003) Dietary (n-3) polyunsaturated fatty acids remodel mouse T-cell lipid rafts. J Nutr 133: 1913-1920.
36. Owen M, Triffitt JT, (1976) Extravascular albumin in bone tissue. J Physiol 257: 293-307.
37. McCarthy ID, (1997) Clearance of albumin by cortical bone and marrow. Clin Orthop Relat Res pp. 24-29.
38. Sun D, Krishnan A, Zaman K, Lawrence R, Bhattacharya A, et al. (2003) Dietary n-3 fatty acids decrease osteoclastogenesis and loss of bone mass in ovariectomized mice. J Bone Miner Res 18: 1206-1216.
39. Moitra J, Mason MM, Olive M, Krylov D, Gavrilova O, et al. (1998) Life without white fat: a transgenic mouse. Genes Dev 12: 3168-3181.
40. Wang J, Wu X, Simonavicius N, Tian H, Ling L, (2006) Medium-chain fatty acids as ligands for orphan G protein-coupled receptor GPR84. J Biol Chem 281: 34457-34464.
41. Hoak JC, Spector AA, Fry GL, Warner ED, (1970) Effect of free fatty acids on ADP-induced platelet aggregation. Nature 228: 1330-1332.
42. Anderson WB, Jaworski CJ, (1977) Modulation of adenylate cyclase activity of fibroblasts by free fatty acids and phospholipids. Arch Biochem Biophys 180: 374-383.
43. Thomas P, Smart TG, (2005) HEK293 cell line: a vehicle for the expression of recombinant proteins. J Pharmacol Toxicol Methods 51: 187-200.
44. Sneddon WB, Yang YM, Ba JM, Harinstein LM, Friedman PA, (2007) Extracellular signal-regulated kinase activation by parathyroid hormone in distal tubule cells. Am J Physiol-Renal 292: F1028-F1034.
45. Wang D, Christensen K, Chawla K, Xiao G, Krebsbach PH, et al. (1999) Isolation and characterization of MC3T3-E1 preosteoblast subclones with distinct in vitro and in vivo differentiation/mineralization potential. J Bone Miner Res 14: 893-903.
46. Klausner RD, Kleinfeld AM, Hoover RL, Karnovsky MJ, (1980) Lipid domains in membranes. Evidence derived from structural perturbations induced by free fatty acids and lifetime heterogeneity analysis. J Biol Chem 255: 1286-1295.
47. Otto JC, Smith WL, (1994) The orientation of prostaglandin endoperoxide synthases-1 and-2 in the endoplasmic reticulum. J Biol Chem 269: 19868-19875.
48. Saito J, Terano T, Hirai A, Shiina T, Tamura Y, et al. (1997) Mechanisms of enhanced production of PGI2 in cultured rat vascular smooth muscle cells enriched with eicosapentaenoic acid. Atherosclerosis 131: 219-228.
49. Kulmacz RJ, Pendleton RB, Lands WE, (1994) Interaction between peroxidase and cyclooxygenase activities in prostaglandin-endoperoxide synthase. Interpretation of reaction kinetics. J Biol Chem 269: 5527-5536.
50. Zhang YL, Frangos JA, Chachisvilis M, (2009) Mechanical stimulus alters conformation of type 1 parathyroid hormone receptor in bone cells. Am J Physiol-Cell Ph 296: C1391-C1399.
51. Nutt RF, Caulfield MP, Levy JJ, Gibbons SW, Rosenblatt M, et al. (1990) Removal of partial agonism from parathyroid hormone (PTH)-related protein-(7-34)NH2 by substitution of PTH amino acids at positions 10 and 11. Endocrinology 127: 491-493.
52. Chou TC, Talalay P, (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22: 27-55.
53. Chou TC, (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58: 621-681.
54. Gesty-Palmer D, Chen M, Reiter E, Ahn S, Nelson CD, et al. (2006) Distinct beta-arrestin- and G protein-dependent pathways for parathyroid hormone receptor-stimulated ERK1/2 activation. J Biol Chem 281: 10856-10864.
55. Vilardaga JP, Steinmeyer R, Harms GS, Lohse MJ, (2005) Molecular basis of inverse agonism in a G protein-coupled receptor. Nat Chem Biol 1: 25-28.
56. Castro M, Nikolaev VO, Palm D, Lohse MJ, Vilardaga JP, (2005) Turn-on switch in parathyroid hormone receptor by a two-step parathyroid hormone binding mechanism. Proc Natl Acad Sci U S A 102: 16084-16089.
57. Rossi AM, Taylor CW, (2011) Analysis of protein-ligand interactions by fluorescence polarization. Nat Protoc 6: 365-387.
58. Dean T, Linglart A, Mahon MJ, Bastepe M, Juppner H, et al. (2006) Mechanisms of ligand binding to the parathyroid hormone (PTH)/PTH-related protein receptor: selectivity of a modified PTH(1-15) radioligand for GalphaS-coupled receptor conformations. Mol Endocrinol 20: 931-943.
59. Cheng HC, (2001) The power issue: determination of KB or Ki from IC50. A closer look at the Cheng-Prusoff equation, the Schild plot and related power equations. J Pharmacol Toxicol Methods 46: 61-71.
60. Jilka RL, Weinstein RS, Bellido T, Roberson P, Parfitt AM, et al. (1999) Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest 104: 439-446.
61. Jilka RL, Weinstein RS, Bellido T, Parfitt AM, Manolagas SC, (1998) Osteoblast programmed cell death (apoptosis): modulation by growth factors and cytokines. J Bone Miner Res 13: 793-802.
62. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, et al. (2003) The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278: 11312-11319.
63. Le Poul E, Loison C, Struyf S, Springael JY, Lannoy V, et al. (2003) Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 278: 25481-25489.
64. Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, et al. (2005) Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 11: 90-94.
65. Stoddart LA, Smith NJ, Milligan G, (2008) International Union of Pharmacology. LXXI. Free fatty acid receptors FFA1,-2, and-3: pharmacology and pathophysiological functions. Pharmacol Rev 60: 405-417.
66. Qin L, Raggatt LJ, Partridge NC, (2004) Parathyroid hormone: a double-edged sword for bone metabolism. Trends Endocrinol Metab 15: 60-65.
67. Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, et al. (2010) GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 142: 687-698.
68. Xiao G, Jiang D, Thomas P, Benson MD, Guan K, et al. (2000) MAPK pathways activate and phosphorylate the osteoblast-specific transcription factor, Cbfa1. J Biol Chem 275: 4453-4459.
69. Sowa H, Kaji H, Yamaguchi T, Sugimoto T, Chihara K, (2002) Activations of ERK1/2 and JNK by transforming growth factor beta negatively regulate Smad3-induced alkaline phosphatase activity and mineralization in mouse osteoblastic cells. J Biol Chem 277: 36024-36031.
70. Smith E, Frenkel B, (2005) Glucocorticoids inhibit the transcriptional activity of LEF/TCF in differentiating osteoblasts in a glycogen synthase kinase-3beta-dependent and-independent manner. J Biol Chem 280: 2388-2394.
71. Zacharias DA, Violin JD, Newton AC, Tsien RY, (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296: 913-916.
72. Chachisvilis M, Zhang YL, Frangos JA, (2006) G protein-coupled receptors sense fluid shear stress in endothelial cells. Proc Natl Acad Sci U S A 103: 15463-15468.